Abstract
Totipotency is the ability of a cell to regenerate the entire organism, even after previous differentiation as a specific cell. When totipotency is coupled with active cell division, it was presumed that cell division is essential for this expression. Here, using the stress-induction system of somatic embryos in carrots, we show that cell division is not essential for the expression of totipotency in somatic/embryonic conversion. Morphological and histochemical analyses showed that the cell did not divide during embryo induction. Inhibitors of cell division did not affect the rate of somatic embryo formation. Our results indicate that the newly acquired trait of differentiation appears without cell division, but does not arise with cell division as a newborn cell.
Similar content being viewed by others
Abbreviations
- AP:
-
Aphidicolin
- BrdU:
-
5-Bromo-2-deoxyuridine
- DAIP:
-
4′,6-Diamidino-2-phenylindole
- DMSO:
-
Dimethyl sulfoxide
- FdU:
-
5-Fluoro-2′-deoxyuridine
- PP:
-
Propyzamide
References
Asahina M, Iwai H, Kikuchi A, Yamaguchi S, Kamiya Y, Kamada H, Satoh S (2002) Gibberellin produced in the cotyledon is required for cell division during tissue reunion in the cortex of cut cucumber and tomato hypocotyls. Plant Physiol 129:201–210
Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154–156
Fukuda H, Komamine A (1980) Establishment of an experimental system for the study of tracheary element differentiation from single cells isolated from the mesophyll of Zinnia elegans. Plant Physiol 65:57–60
Fukuda H, Komamine A (1981) Relationship between tracheary element differentiation and the cell cycle in single cells isolated from the mesophyll of Zinnia elegans. Physiol Plant 52:423–430
Gao S, Chung YG, Parseghian MH, King GJ, Adashi EY, Latham KE (2004) Rapid H1 linker histone transitions following fertilization or somatic cell nuclear transfer, evidence for a uniform developmental program in mice. Dev Biol 266:62–75
Ikeda-Iwai M, Umehara M, Satoh S, Kamada H (2003) Stress-induced somatic embryogenesis in vegetative tissues of Arabidopsis thaliana. Plant J 34:107–114
Illmensee K, Mintz B (1976) Totipotency and normal differentiation of single teratocarcinoma cells cloned by injection into blastocysts. Proc Natl Acad Sci USA 73:549–553
Kamada H, Harada H (1979) Studies on organogenesis in carrot tissue culture. I. Effects of growth regulation on somatic embryogenesis and root formation. Z Pflanzenphysiol 91:225–266
Kamada H, Kobayashi K, Kiyosue T, Harada H (1989) Stress-induced somatic embryogenesis in carrot and its application to synthetic seed production. In Vitro Cell Dev Biol 25:1163–1166
Kamada H, Tachikawa Y, Saitou T, Harada H (1994) Heat stress induction of carrot somatic embryogenesis. Plant Tissue Cult Lett 11:229–232
Kates JR, Jones RF (1964) The control of gametic differentiation in liquid cultures of Chlamydomonas. J Cell Comp Physiol 63:157–164
Kikuchi A, Sanuki N, Higashi K, Koshiba T, Kamada H (2006) Abscisic acid and stress treatment are essential for the acquisition of embryogenic competence by carrot somatic cells. Planta 223:637–645
Kiyosue T, Kamada H, Harada H (1989) Induction of somatic embryogenesis by salt stress in carrot. Plant Tissue Cult Lett 6:162–164
Kiyosue T, Takano K, Kamada H, Harada H (1990) Induction of somatic embryogenesis in carrot by heavy metal ions. Can J Bot 68:2021–2033
Kiyosue T, Yamaguchi-Shinozaki K, Shinozaki K, Kamada H, Harada H (1993) cDNA cloning of ECP40, an embryogenic-cell protein in carrot, and its expression during somatic and zygotic embryogenesis. Plant Mol Biol 21:1053–1068
Kumlehn J, Loerz H (1999) Monitoring sporophytic development of individual microspores of barley (Hordeum vulgare L.). In: Clement C, Paccini E, Audran JC (eds) Anther and pollen, from biology to biotechnology. Springer, Berlin, pp 183–190
Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
Nagata T, Nemoto Y, Hasezawa S (1992) Tobacco BY-2 cell line as the “HeLa” cell in the cell biology of higher plants. Int Rev Cytol 132:1–30
Nomura K, Komamine A (1985) Identification and isolation of single cells that produce somatic embryos at a high frequency in a carrot suspension culture. Plant Physiol 79:988–991
Reinert J (1958) Morphogenese und ihre Kontrolle an Gewebekulturen aus Carotten. Naturwissenschaften 45:344–345
Samuels AL, Meehl J, Lipe M, Staehelin LA (1998) Optimizing conditions for tobacco BY-2 cell cycle synchronization. Protoplasma 202:232–236
Santos F, Dean W (2004) Epigenetic reprogramming during early development in mammals. Reproduction 127:643–651
Santos TA, Dias C, Henriques P, Brito R, Barbosa A, Regateiro F, Santos AA (2003) Cytogenetic analysis of spontaneously activated noninseminated oocytes and parthenogenetically activated failed fertilized human oocytes—implications for the use of primate parthenotes for stem cell production. J Assist Reprod Genet 20:122–130
Shibukawa T, Yazawa K, Kikuchi A, Kamada H (2009) Possible involvement of DNA methylation on expression regulation of carrot LEC1 gene in its 5′-upstream region. Gene 437:22–31
Skoog F, Miller CO (1957) Chemical regulation of growth and organ formation in plant tissue cultured in vitro. Symp Soc Exp Biol 11:118–130
Steward FC, Mapes MO, Smith J (1958) Growth and organized development of cultured cells. I. Growth and division of freely suspended cells. Am J Bot 45:707–708
Suzuki T, Sasaki N, Sakai A, Kawano S, Kuroiwa T (1995) Localization of organelle DNA synthesis within the root apical meristem of rice. J Exp Bot 46:19–25
Tanaka M, Kikuchi A, Kamada H (2008) The Arabidopsis histone deacetylases HDA6 and HDA19 contribute to the repression of embryonic properties after germination. Plant Physiol 146:149–161
Tanaka M, Kikuchi A, Kamada H (2009) Isolation of putative embryo-specific genes using stress induction of carrot somatic embryos. Breed Sci 59:37–46
Teranishi T, Tanaka M, Kimoto S, Ono Y, Miyakoshi K, Kono T, Yoshimura Y (2004) Rapid replacement of somatic linker histones with the oocyte-specific linker histone H1foo in nuclear transfer. Dev Biol 266:76–86
Wakayama T, Perry AC, Zuccotti M, Johnson KR, Yanagimachi R (1998) Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 394:369–374
Wilde HD, Nelson WS, Booij H, De Vries SC, Thomas TL (1988) Gene-expression programs in embryogenic and non-embryogenic carrot cultures. Planta 176:205–211
Wilmut I, Schnieke AE, McWhir J, Kind AJ, Campbell KH (1997) Viable offspring derived from fetal and adult mammalian cells. Nature 385:810–813 (erratum in Nature 386:200)
Yazawa K, Takahata K, Kamada H (2004) Isolation of the gene encoding carrot leafy cotyledon1 and expression analysis during somatic zygotic embryogenesis. Plant Physiol Biochem 42:215–223
Zhang L, Qiu Z, Hu Y, Yang F, Yan S, Zhao L, Li B, He S, Huang M, Li J, Li L (2011) ABA treatment of germinating maize seeds induces VP1 gene expression and selective promoter-associated histone acetylation. Physiol Plant 143:287–296
Acknowledgments
This work was supported in part by the Grants-in-Aid program from the Ministry of Education, Culture, Sports, Science and Technology of Japan (Grant no. 23570045) and by the joint research program “Plant Transgenic Research Design, University of Tsukuba.”
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Kikuchi, A., Asahina, M., Tanaka, M. et al. Acquisition of embryogenic competency does not require cell division in carrot somatic cell. J Plant Res 126, 243–250 (2013). https://doi.org/10.1007/s10265-012-0517-3
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10265-012-0517-3